Age-associated aberrations of the cumulus-oocyte interaction and in the zona pellucida structure reduce fertility in female mice

Abstract, One of the major age-related declines in female reproductive function is the reduced quantity and quality of oocytes. Here we demonstrate that structural changes in the zona pellucida (ZP) were associated with decreased fertilization rates from 34- to 38-week-old female mice, equivalent to...

Full description

Saved in:
Bibliographic Details
Main Authors: Yu Ishikawa-Yamauchi, Chihiro Emori, Hideto Mori, Tsutomu Endo, Kiyonori Kobayashi, Yuji Watanabe, Hiroshi Sagara, Takeshi Nagata, Daisuke Motooka, Akinori Ninomiya, Manabu Ozawa, Masahito Ikawa
Format: Article
Language:English
Published: Nature Portfolio 2024-12-01
Series:Communications Biology
Online Access:https://doi.org/10.1038/s42003-024-07305-z
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1846101017602555904
author Yu Ishikawa-Yamauchi
Chihiro Emori
Hideto Mori
Tsutomu Endo
Kiyonori Kobayashi
Yuji Watanabe
Hiroshi Sagara
Takeshi Nagata
Daisuke Motooka
Akinori Ninomiya
Manabu Ozawa
Masahito Ikawa
author_facet Yu Ishikawa-Yamauchi
Chihiro Emori
Hideto Mori
Tsutomu Endo
Kiyonori Kobayashi
Yuji Watanabe
Hiroshi Sagara
Takeshi Nagata
Daisuke Motooka
Akinori Ninomiya
Manabu Ozawa
Masahito Ikawa
author_sort Yu Ishikawa-Yamauchi
collection DOAJ
description Abstract, One of the major age-related declines in female reproductive function is the reduced quantity and quality of oocytes. Here we demonstrate that structural changes in the zona pellucida (ZP) were associated with decreased fertilization rates from 34- to 38-week-old female mice, equivalent to the mid-reproductive of human females. In middle-aged mouse ovaries, the decline in the number of transzonal projections was accompanied by a decrease in cumulus cell-oocyte interactions, resulting in a deterioration of the oocyte quality. Scanning electron microscopy showed the ZP surface microfilament structure transitioning from rugged to smooth with aging, leading to decreased fertilization rates due to impaired sperm binding to the ZP. Moreover, the fertilization rate of middle-aged mice was restored to a comparable level to that of young mice by destabilizing the ZP in the presence of glutathione. These results suggest that the age-related structural changes in the ZP are key for successful fertilization at reproductive age.
format Article
id doaj-art-f9c910b7931e4c4d8bbc2901d36b7a86
institution Kabale University
issn 2399-3642
language English
publishDate 2024-12-01
publisher Nature Portfolio
record_format Article
series Communications Biology
spelling doaj-art-f9c910b7931e4c4d8bbc2901d36b7a862024-12-29T12:41:11ZengNature PortfolioCommunications Biology2399-36422024-12-017111410.1038/s42003-024-07305-zAge-associated aberrations of the cumulus-oocyte interaction and in the zona pellucida structure reduce fertility in female miceYu Ishikawa-Yamauchi0Chihiro Emori1Hideto Mori2Tsutomu Endo3Kiyonori Kobayashi4Yuji Watanabe5Hiroshi Sagara6Takeshi Nagata7Daisuke Motooka8Akinori Ninomiya9Manabu Ozawa10Masahito Ikawa11The Institute of Medical Science, The University of TokyoResearch Institute for Microbial Diseases, Osaka UniversityInstitute for Advanced Biosciences, Keio UniversityResearch Institute for Microbial Diseases, Osaka UniversityResearch Institute for Microbial Diseases, Osaka UniversityThe Institute of Medical Science, The University of TokyoThe Institute of Medical Science, The University of TokyoSchool of Integrative and Global Majors, University of TsukubaResearch Institute for Microbial Diseases, Osaka UniversityResearch Institute for Microbial Diseases, Osaka UniversityThe Institute of Medical Science, The University of TokyoThe Institute of Medical Science, The University of TokyoAbstract, One of the major age-related declines in female reproductive function is the reduced quantity and quality of oocytes. Here we demonstrate that structural changes in the zona pellucida (ZP) were associated with decreased fertilization rates from 34- to 38-week-old female mice, equivalent to the mid-reproductive of human females. In middle-aged mouse ovaries, the decline in the number of transzonal projections was accompanied by a decrease in cumulus cell-oocyte interactions, resulting in a deterioration of the oocyte quality. Scanning electron microscopy showed the ZP surface microfilament structure transitioning from rugged to smooth with aging, leading to decreased fertilization rates due to impaired sperm binding to the ZP. Moreover, the fertilization rate of middle-aged mice was restored to a comparable level to that of young mice by destabilizing the ZP in the presence of glutathione. These results suggest that the age-related structural changes in the ZP are key for successful fertilization at reproductive age.https://doi.org/10.1038/s42003-024-07305-z
spellingShingle Yu Ishikawa-Yamauchi
Chihiro Emori
Hideto Mori
Tsutomu Endo
Kiyonori Kobayashi
Yuji Watanabe
Hiroshi Sagara
Takeshi Nagata
Daisuke Motooka
Akinori Ninomiya
Manabu Ozawa
Masahito Ikawa
Age-associated aberrations of the cumulus-oocyte interaction and in the zona pellucida structure reduce fertility in female mice
Communications Biology
title Age-associated aberrations of the cumulus-oocyte interaction and in the zona pellucida structure reduce fertility in female mice
title_full Age-associated aberrations of the cumulus-oocyte interaction and in the zona pellucida structure reduce fertility in female mice
title_fullStr Age-associated aberrations of the cumulus-oocyte interaction and in the zona pellucida structure reduce fertility in female mice
title_full_unstemmed Age-associated aberrations of the cumulus-oocyte interaction and in the zona pellucida structure reduce fertility in female mice
title_short Age-associated aberrations of the cumulus-oocyte interaction and in the zona pellucida structure reduce fertility in female mice
title_sort age associated aberrations of the cumulus oocyte interaction and in the zona pellucida structure reduce fertility in female mice
url https://doi.org/10.1038/s42003-024-07305-z
work_keys_str_mv AT yuishikawayamauchi ageassociatedaberrationsofthecumulusoocyteinteractionandinthezonapellucidastructurereducefertilityinfemalemice
AT chihiroemori ageassociatedaberrationsofthecumulusoocyteinteractionandinthezonapellucidastructurereducefertilityinfemalemice
AT hidetomori ageassociatedaberrationsofthecumulusoocyteinteractionandinthezonapellucidastructurereducefertilityinfemalemice
AT tsutomuendo ageassociatedaberrationsofthecumulusoocyteinteractionandinthezonapellucidastructurereducefertilityinfemalemice
AT kiyonorikobayashi ageassociatedaberrationsofthecumulusoocyteinteractionandinthezonapellucidastructurereducefertilityinfemalemice
AT yujiwatanabe ageassociatedaberrationsofthecumulusoocyteinteractionandinthezonapellucidastructurereducefertilityinfemalemice
AT hiroshisagara ageassociatedaberrationsofthecumulusoocyteinteractionandinthezonapellucidastructurereducefertilityinfemalemice
AT takeshinagata ageassociatedaberrationsofthecumulusoocyteinteractionandinthezonapellucidastructurereducefertilityinfemalemice
AT daisukemotooka ageassociatedaberrationsofthecumulusoocyteinteractionandinthezonapellucidastructurereducefertilityinfemalemice
AT akinorininomiya ageassociatedaberrationsofthecumulusoocyteinteractionandinthezonapellucidastructurereducefertilityinfemalemice
AT manabuozawa ageassociatedaberrationsofthecumulusoocyteinteractionandinthezonapellucidastructurereducefertilityinfemalemice
AT masahitoikawa ageassociatedaberrationsofthecumulusoocyteinteractionandinthezonapellucidastructurereducefertilityinfemalemice